Skip to main content
SpringerLink
Log in

Role of ultrasonography in the evaluation of disease severity and treatment efficacy in adenomyosis

  • Review
  • Published:
Archives of Gynecology and Obstetrics Aims and scope Submit manuscript

Abstract

Background

Adenomyosis is a benign disorder characterized by the presence of ectopic endometrial glands and stroma within the myometrium. The main clinical manifestations of adenomyosis are dysmenorrhea, menorrhagia, and infertility, which affect patients’ quality of life. Recently, with advancements in imaging techniques, magnetic resonance imaging, and ultrasonography have become the main diagnostic tools for adenomyosis. In addition to the diagnosis and differential diagnosis of adenomyosis, ultrasonography can also be used to evaluate the severity of adenomyosis. The emergence of new techniques, such as elastography and contrast-enhanced ultrasonography (CEUS), has significantly improved the accuracy of ultrasound-based diagnosis of adenomyosis. These two imaging tools can also be used for the differential diagnosis of adenomyosis and the evaluation of treatment efficacy after medication or ablation procedure.

Objective

we review the efficacy of ultrasonography as a diagnostic tool for adenomyosis. We also aim to introduce the potential of ultrasound imaging in the evaluation of the severity of this disease, as well as the application of elastography and contrast-enhanced ultrasonography (CEUS) in its diagnosis.

Results and Conclusion

Our findings reveal the potential value of ultrasonography combined with elastography and/or CEUS as medication guidance and efficacy evaluation tools in the long-term management of adenomyosis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data Availability

Data availability is not applicable to this article as no new data were created or analyzed in this study

References

  1. Van den Bosch T, Van Schoubroeck D (2018) Ultrasound diagnosis of endometriosis and adenomyosis: State of the art. Best Pract Res Clin Obstet Gynaecol 51:16–24. https://doi.org/10.1016/j.bpobgyn.2018.01.013

    Article  PubMed  Google Scholar 

  2. Cunningham RK, Horrow MM, Smith RJ, Springer J (2018) Adenomyosis: a sonographic diagnosis. Radiographics 38(5):1576–1589. https://doi.org/10.1148/rg.2018180080

    Article  PubMed  Google Scholar 

  3. Harada T, Khine YM, Kaponis A, Nikellis T, Decavalas G, Taniguchi F (2016) The impact of adenomyosis on women’s fertility. Obstet Gynecol Surv 71(9):557–568. https://doi.org/10.1097/ogx.0000000000000346

    Article  PubMed  PubMed Central  Google Scholar 

  4. Vercellini P, Consonni D, Dridi D, Bracco B, Frattaruolo MP, Somigliana E (2014) Uterine adenomyosis and in vitro fertilization outcome: a systematic review and meta-analysis. Hum Reprod 29(5):964–977. https://doi.org/10.1093/humrep/deu041

    Article  PubMed  Google Scholar 

  5. Younes G, Tulandi T (2017) Effects of adenomyosis on in vitro fertilization treatment outcomes: a meta-analysis. Fertil Steril 108(3):483-490.e3. https://doi.org/10.1016/j.fertnstert.2017.06.025

    Article  PubMed  Google Scholar 

  6. Liu X, Ding D, Ren Y, Guo SW (2018) Transvaginal elastosonography as an imaging technique for diagnosing adenomyosis. Reprod Sci 25(4):498–514. https://doi.org/10.1177/1933719117750752

    Article  PubMed  Google Scholar 

  7. Guo SW (2022) Cracking the enigma of adenomyosis: an update on its pathogenesis and pathophysiology. Reproduction 164(5):R101–R121. https://doi.org/10.1530/rep-22-0224

    Article  CAS  PubMed  Google Scholar 

  8. Chapron C, Vannuccini S, Santulli P, Abrão MS, Carmona F, Fraser IS et al (2020) Diagnosing adenomyosis: an integrated clinical and imaging approach. Hum Reprod Update 26(3):392–411. https://doi.org/10.1093/humupd/dmz049

    Article  PubMed  Google Scholar 

  9. Grab D, Merz E, Eichhorn KH, Tutschek B, Kagan KO, Heling KS et al (2022) Basic gynecologic ultrasound examination (Level I): DEGUM, ÖGUM, and SGUM recommendations. Ultraschall Med. https://doi.org/10.1055/a-1851-5157.10.1055/a-1851-515

    Article  PubMed  Google Scholar 

  10. Van den Bosch T, Dueholm M, Leone FP, Valentin L, Rasmussen CK, Votino A et al (2015) Terms, definitions and measurements to describe sonographic features of myometrium and uterine masses: a consensus opinion from the Morphological Uterus Sonographic Assessment (MUSA) group. Ultrasound Obstet Gynecol 46(3):284–298. https://doi.org/10.1002/uog.14806

    Article  PubMed  Google Scholar 

  11. Van den Bosch T, de Bruijn AM, de Leeuw RA, Dueholm M, Exacoustos C, Valentin L et al (2019) Sonographic classification and reporting system for diagnosing adenomyosis. Ultrasound Obstet Gynecol 53(5):576–582. https://doi.org/10.1002/uog.19096

    Article  PubMed  Google Scholar 

  12. Bazot M, Daraï E, Rouger J, Detchev R, Cortez A, Uzan S (2002) Limitations of transvaginal sonography for the diagnosis of adenomyosis, with histopathological correlation. Ultrasound Obstet Gynecol 20(6):605–611. https://doi.org/10.1046/j.1469-0705.2002.00852.x

    Article  CAS  PubMed  Google Scholar 

  13. Levy G, Dehaene A, Laurent N, Lernout M, Collinet P, Lucot JP et al (2013) An update on adenomyosis. Diagn Interv Imaging 94(1):3–25. https://doi.org/10.1016/j.diii.2012.10.012

    Article  CAS  PubMed  Google Scholar 

  14. Dueholm M (2006) Transvaginal ultrasound for diagnosis of adenomyosis: a review. Best practice and research. Best Pract Res Clin Obstet Gynaecol 20(4):569–582. https://doi.org/10.1016/j.bpobgyn.2006.01.005

    Article  PubMed  Google Scholar 

  15. Liu L, Li W, Leonardi M, Condous G, Da Silva CF, Mol BW et al (2021) Diagnostic accuracy of transvaginal ultrasound and magnetic resonance imaging for adenomyosis: systematic review and meta-analysis and review of sonographic diagnostic criteria. J Ultrasound Med 40(11):2289–2306. https://doi.org/10.1002/jum.15635

    Article  PubMed  Google Scholar 

  16. Rasmussen CK, Hansen ES, Dueholm M (2019) Inter-rater agreement in the diagnosis of adenomyosis by 2- and 3-dimensional transvaginal ultrasonography. J Ultrasound Med 38(3):657–666. https://doi.org/10.1002/jum.14735

    Article  PubMed  Google Scholar 

  17. Exacoustos C, Brienza L, Di Giovanni A, Szabolcs B, Romanini ME, Zupi E et al (2011) Adenomyosis: three-dimensional sonographic findings of the junctional zone and correlation with histology. Ultrasound Obstet Gynecol 37(4):471–479. https://doi.org/10.1002/uog.8900

    Article  CAS  PubMed  Google Scholar 

  18. Andres MP, Borrelli GM, Ribeiro J, Baracat EC, Abrão MS, Kho RM (2018) Transvaginal ultrasound for the diagnosis of adenomyosis: systematic review and meta-analysis. J Minim Invasive Gynecol 25(2):257–264. https://doi.org/10.1016/j.jmig.2017.08.653

    Article  PubMed  Google Scholar 

  19. Kepkep K, Tuncay YA, Göynümer G, Tutal E (2007) Transvaginal sonography in the diagnosis of adenomyosis: which findings are most accurate? Ultrasound Obstet Gynecol 30(3):341–345. https://doi.org/10.1002/uog.3985

    Article  CAS  PubMed  Google Scholar 

  20. Rasmussen CK, Van den Bosch T, Exacoustos C, Manegold-Brauer G, Benacerraf BR, Froyman W et al (2019) Intra- and inter-rater agreement describing myometrial lesions using morphologic uterus sonographic assessment: a pilot study. J Ultrasound Med 38(10):2673–2683. https://doi.org/10.1002/jum.14971

    Article  PubMed  Google Scholar 

  21. Harmsen MJ, Van den Bosch T, de Leeuw RA, Dueholm M, Exacoustos C, Valentin L et al (2022) Consensus on revised definitions of Morphological Uterus Sonographic Assessment (MUSA) features of adenomyosis: results of modified Delphi procedure. Ultrasound Obstet Gynecol 60(1):118–131. https://doi.org/10.1002/uog.24786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Keckstein J, Hoopmann M, Merz E, Grab D, Weichert J, Helmy-Bader S et al (2023) Expert opinion on the use of transvaginal sonography for presurgical staging and classification of endometriosis. Arch Gynecol Obstet 307(1):5–19. https://doi.org/10.1007/s00404-022-06766-z

    Article  CAS  PubMed  Google Scholar 

  23. Cohen Ben-Meir L, Soriano D, Zajicek M, Yulzari V, Bouaziz J, Beer-Gabel M et al (2022) The association between gastrointestinal Symptoms and Transvaginal Ultrasound Findings in women referred for endometriosis evaluation: a prospective pilot study. Ultraschall Med 43(5):e81–e89. https://doi.org/10.1055/a-1300-188725

    Article  PubMed  Google Scholar 

  24. Bourdon M, Oliveira J, Marcellin L, Santulli P, Bordonne C, Maitrot Mantelet L et al (2021) Adenomyosis of the inner and outer myometrium are associated with different clinical profiles. Hum Reprod 36(2):349–357. https://doi.org/10.1093/humrep/deaa307

    Article  CAS  PubMed  Google Scholar 

  25. Marques ALS, Andres MP, Mattos LA, Gonçalves MO, Baracat EC, Abrão MS (2021) Association of 2D and 3D transvaginal ultrasound findings with adenomyosis in symptomatic women of reproductive age: a prospective study. Clinics (Sao Paulo) 76:e2981. https://doi.org/10.6061/clinics/2021/e2981

    Article  PubMed  Google Scholar 

  26. Exacoustos C, Lazzeri L, Martire FG, Russo C, Martone S, Centini G et al (2022) Ultrasound findings of Adenomyosis in Adolescents: type and grade of the disease. J Minim Invasive Gynecol 29(2):291-299.e1. https://doi.org/10.1016/j.jmig.2021.08.023

    Article  PubMed  Google Scholar 

  27. Naftalin J, Hoo W, Nunes N, Holland T, Mavrelos D, Jurkovic D (2016) Association between ultrasound features of adenomyosis and severity of menstrual pain. Ultrasound Obstet Gynecol 47(6):779–783. https://doi.org/10.1002/uog.15798

    Article  CAS  PubMed  Google Scholar 

  28. Naftalin J, Hoo W, Pateman K, Mavrelos D, Foo X, Jurkovic D (2014) Is adenomyosis associated with menorrhagia? Hum Reprod 29(3):473–479. https://doi.org/10.1093/humrep/det451

    Article  CAS  PubMed  Google Scholar 

  29. Pinzauti S, Lazzeri L, Tosti C, Centini G, Orlandini C, Luisi S et al (2015) Transvaginal sonographic features of diffuse adenomyosis in 18–30-year-old nulligravid women without endometriosis: association with symptoms. Ultrasound Obstet Gynecol 46(6):730–736. https://doi.org/10.1002/uog.14834

    Article  CAS  PubMed  Google Scholar 

  30. Lazzeri L, Morosetti G, Centini G, Monti G, Zupi E, Piccione E et al (2018) A sonographic classification of adenomyosis: interobserver reproducibility in the evaluation of type and degree of the myometrial involvement. Fertil Steril 110(6):1154-1161.e3. https://doi.org/10.1016/j.fertnstert.2018.06.031

    Article  PubMed  Google Scholar 

  31. Exacoustos C, Morosetti G, Conway F, Camilli S, Martire FG, Lazzeri L et al (2020) New sonographic classification of Adenomyosis: do type and degree of Adenomyosis correlate to severity of symptoms? J Minim Invasive Gynecol 27(6):1308–1315. https://doi.org/10.1016/j.jmig.2019.09.788

    Article  PubMed  Google Scholar 

  32. Tamura H, Kishi H, Kitade M, Asai-Sato M, Tanaka A, Murakami T et al (2017) Complications and outcomes of pregnant women with adenomyosis in Japan. Reprod Med Biol 16(4):330–336. https://doi.org/10.1002/rmb2.1205034

    Article  PubMed  PubMed Central  Google Scholar 

  33. Shiina T, Nightingale KR, Palmeri ML, Hall TJ, Bamber JC, Barr RG et al (2015) WFUMB guidelines and recommendations for clinical use of ultrasound elastography: part 1: basic principles and terminology. Ultrasound Med Biol 41(5):1126–1147. https://doi.org/10.1016/j.ultrasmedbio.2015.03.009

    Article  PubMed  Google Scholar 

  34. Cosgrove D, Piscaglia F, Bamber J, Bojunga J, Correas JM, Gilja OH et al (2013) EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography Part 2: clinical applications. Ultraschall Med 34(3):238–253. https://doi.org/10.1055/s-0033-1335375

    Article  CAS  PubMed  Google Scholar 

  35. Xholli A, Londero APP, Cavalli E, Scovazzi U, Ferraro MF, Vacca I et al (2023) The benefit of transvaginal elastography in detecting deep endometriosis: a feasibility study. Ultraschall Med. https://doi.org/10.1055/a-2028-8214.10.1055/a-2028-821437

    Article  PubMed  Google Scholar 

  36. Săsăran V, Turdean S, Gliga M, Ilyes L, Grama O, Muntean M et al (2021) Value of Strain-ratio elastography in the diagnosis and differentiation of uterine fibroids and adenomyosis. J Pers Med 11(8):824. https://doi.org/10.3390/jpm11080824

    Article  PubMed  PubMed Central  Google Scholar 

  37. Görgülü FF, Okçu NT (2021) Which imaging method is better for the differentiation of adenomyosis and uterine fibroids? J Gynecol Obstet Hum Reprod 50(5):102002. https://doi.org/10.1016/j.jogoh.2020.102002

    Article  PubMed  Google Scholar 

  38. Wei Q, Yan YJ, Wu GG, Ye XR, Jiang F, Liu J et al (2021) Added value of a new strain elastography technique in conventional ultrasound for the diagnosis of breast masses: a prospective multicenter study. Front Oncol 11:779612. https://doi.org/10.3389/fonc.2021.779612

    Article  PubMed  PubMed Central  Google Scholar 

  39. Săsăran V, Turdean S, Mărginean C, Gliga M, Ilyes L, Grama O et al (2022) Transvaginal ultrasound combined with strain-ratio elastography for the concomitant diagnosis of uterine fibroids and adenomyosis: a pilot study. J Clin Med 11(13):3757. https://doi.org/10.3390/jcm11133757

    Article  PubMed  PubMed Central  Google Scholar 

  40. Acar S, Millar E, Mitkova M, Mitkov V (2016) Value of ultrasound shear wave elastography in the diagnosis of adenomyosis. Ultrasound 24(4):205–213. https://doi.org/10.1177/1742271X16673677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Frank ML, Schäfer SD, Möllers M, Falkenberg MK, Braun J, Möllmann U et al (2016) Importance of transvaginal elastography in the diagnosis of uterine fibroids and adenomyosis. Ultraschall Med 37(4):373–378. https://doi.org/10.1055/s-0035-1553266

    Article  CAS  PubMed  Google Scholar 

  42. Tessarolo M, Bonino L, Camanni M, Deltetto F (2011) Elastosonography: a possible new tool for diagnosis of adenomyosis? Eur Radiol 21(7):1546–1552. https://doi.org/10.1007/s00330-011-2064-z

    Article  PubMed  Google Scholar 

  43. Wang XL, Lin S, Lyu GR (2012) Advances in the clinical application of ultrasound elastography in uterine imaging. Insights Imag 13(1):141. https://doi.org/10.1186/s13244-022-01274-9

    Article  Google Scholar 

  44. Wang S, Li B, Duan H, Wang Y, Shen X, Dong Q (2021) Abnormal expression of connective tissue growth factor and its correlation with fibrogenesis in adenomyosis. Reprod Biomed Online 42(3):651–660. https://doi.org/10.1016/j.rbmo.2020.11.002

    Article  CAS  PubMed  Google Scholar 

  45. Yang B, Gu N, Shi S, Zhang C, Chen L, Ouyang J et al (2021) Immunoreactivity of plasminogen activator inhibitor 1 and Its correlation with dysmenorrhea and lesional fibrosis in adenomyosis. Reprod Sci 28(8):2378–2386. https://doi.org/10.1007/s43032-021-00513-6

    Article  CAS  PubMed  Google Scholar 

  46. Huang Q, Liu X, Critchley H, Fu Z, Guo SW (2022) How does the extent of fibrosis in adenomyosis lesions contribute to heavy menstrual bleeding? Reprod Med Biol 21(1):e12442. https://doi.org/10.1002/rmb2.12442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Xie M, Yu H, Zhang X, Wang W, Ren Y (2019) Elasticity of adenomyosis is increased after GnRHa therapy and is associated with spontaneous pregnancy in infertile patents. J Gynecol Obstet Hum Reprod 48(10):849–853. https://doi.org/10.1016/j.jogoh.2019.05.003

    Article  PubMed  Google Scholar 

  48. Marigliano C, Panzironi G, Molisso L, Pizzuto A, Ciolina F, Napoli A et al (2016) First experience of real-time elastography with transvaginal approach in assessing response to MRgFUS treatment of uterine fibroids. Radiol Med 121(12):926–934. https://doi.org/10.1007/s11547-016-0679-5

    Article  PubMed  Google Scholar 

  49. Chhabra P, Daugherty R, LeNoir AM, Grilli C, Makai G, Patel N et al (2021) Comparison of contrast-enhanced ultrasound versus magnetic resonance imaging in the detection and characterization of Uterine Leiomyomas. J Ultrasound Med 40(6):1147–1153. https://doi.org/10.1002/jum.15495

    Article  PubMed  Google Scholar 

  50. Zhang YQ, Chen JH, Zhu TT, Zhao AX, Zhuang LT, Lu CY et al (2022) Applying contrast-enhanced ultrasound model to distinguish atypical focal adenomyosis from uterine leiomyomas. Ann Transl Med 10(20):1108

    Article  PubMed  PubMed Central  Google Scholar 

  51. Durot I, Wilson SR, Willmann JK (2018) Contrast-enhanced ultrasound of malignant liver lesions. Abdom Radiol (NY) 43(4):819–847. https://doi.org/10.1007/s00261-017-1360-8

    Article  PubMed  Google Scholar 

  52. Liu X, Jang HJ, Khalili K, Kim TK, Atri M (2018) Successful Integration of contrast-enhanced US into routine abdominal imaging. Radiographics 38(5):1454–1477. https://doi.org/10.1148/rg.2018170152

    Article  PubMed  Google Scholar 

  53. Pang T, Huang L, Deng Y, Wang T, Chen S, Gong X et al (2017) Logistic regression analysis of conventional ultrasonography, strain elastosonography, and contrast-enhanced ultrasound characteristics for the differentiation of benign and malignant thyroid nodules. PLoS ONE 12(12):e0188987. https://doi.org/10.1371/journal.pone.0188987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Green RW, Epstein E (2020) Dynamic contrast-enhanced ultrasound improves diagnostic performance in endometrial cancer staging. Ultrasound Obstet Gynecol 56(1):96–105. https://doi.org/10.1002/uog.21885

    Article  CAS  PubMed  Google Scholar 

  55. Dietrich CF (2019) Contrast-Enhanced Ultrasound of Benign Focal Liver Lesions. Ultraschall Med 40(1):12–29. https://doi.org/10.1055/a-0668-5746

    Article  PubMed  Google Scholar 

  56. Ma X, Zhao Y, Zhang B, Ling W, Zhuo H, Jia H et al (2015) Contrast-enhanced ultrasound for differential diagnosis of malignant and benign ovarian tumors: systematic review and meta-analysis. Ultrasound Obstet Gynecol 46(3):277–283. https://doi.org/10.1002/uog.14800

    Article  CAS  PubMed  Google Scholar 

  57. Peng S, Xiong Y, Li K, He M, Deng Y, Chen L et al (2012) Clinical utility of a microbubble-enhancing contrast (“SonoVue”) in treatment of uterine fibroids with high intensity focused ultrasound: a retrospective study. Eur J Radiol 81(12):3832–3838. https://doi.org/10.1016/j.ejrad.2012.04.030

    Article  PubMed  Google Scholar 

  58. Jiang N, Xie B, Zhang X, He M, Li K, Bai J et al (2014) Enhancing ablation effects of a microbubble-enhancing contrast agent (“SonoVue”) in the treatment of uterine fibroids with high-intensity focused ultrasound: a randomized controlled trial. Cardiovasc Intervent Radiol 37(5):1321–1328. https://doi.org/10.1007/s00270-013-0803-z

    Article  PubMed  Google Scholar 

  59. Wang W, Wang Y, Tang J (2009) Safety and efficacy of high intensity focused ultrasound ablation therapy for adenomyosis. Acad Radiol 16(11):1416–1423. https://doi.org/10.1016/j.acra.2009.06.005

    Article  PubMed  Google Scholar 

  60. Xu C, Tang Y, Zhao Y, Li Y, Feng Q (2020) Use of contrast-enhanced ultrasound in evaluating the efficacy and application value of microwave ablation for adenomyosis. J Cancer Res Ther 16(2):365–371. https://doi.org/10.4103/jcrt.jcrt_769_18

    Article  PubMed  Google Scholar 

  61. Cheng CQ, Zhang RT, Xiong Y, Chen L, Wang J, Huang GH et al (2015) Contrast-enhanced ultrasound for evaluation of high-intensity focused ultrasound treatment of benign uterine diseases: retrospective analysis of contrast safety. Medicine (Baltimore) 94(16):e729. https://doi.org/10.1097/MD.0000000000000729

    Article  PubMed  Google Scholar 

Download references

Funding

This work was funded by the National Key R&D Program of China (Grant No. 2022YFC2704002), National Natural Science Foundation of China (Grant No. 82071621), and Major Basic Research of Natural Science Foundation of Shandong Province (Grant No. ZR2021ZD34).

Author information

Authors and Affiliations

  1. Department of Obstetrics and Gynecology, Shandong Provincial Hospital, Jinan, 250000, Shandong, China

    Qianhui Ren, Ming Yuan & Guoyun Wang

  2. Cheeloo College of Medicine, Shandong University, Jinan, Shandong, China

    Qianhui Ren

  3. Gynecology Laboratory, Shandong Provincial Hospital, Jinan, Shandong, China

    Ming Yuan & Guoyun Wang

Authors
  1. Qianhui Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ming Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guoyun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

RQ: manuscript writing and literature review; YM: manuscript writing and editing; GW: manuscript writing and editing, and project development.

Corresponding author

Correspondence to Guoyun Wang.

Ethics declarations

Conflicts of interest

The authors have no relevant financial or non-financial interests to disclose.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ren, Q., Yuan, M. & Wang, G. Role of ultrasonography in the evaluation of disease severity and treatment efficacy in adenomyosis. Arch Gynecol Obstet 309, 363–371 (2024). https://doi.org/10.1007/s00404-023-07034-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00404-023-07034-4

Keywords

Search

Navigation